Opportunistic consumption of coral spawn by the ruby brittle star (Ophioderma rubicundum)

Abstract Many reef invertebrates reproduce through simultaneous broadcast spawning, with an apparent advantage of overwhelming potential predators and maximizing propagule survival. Although reef fish have been observed to consume coral gamete bundles during spawning events, there are few records of such predation by benthic invertebrates. Here, we document several instances of the ruby brittle star, Ophioderma rubicundum, capturing and consuming egg‐sperm bundles of the mountainous star coral, Orbicella faveolata, and the symmetrical brain coral, Pseudodiploria strigosa, during spawning events in the Cayman Islands in 2012 and the Florida Keys in 2022. These observations are widely separated in space and time (>600 km, 10 years), suggesting that this behavior may be prevalent on western Atlantic reefs. Since O. rubicundum spawns on the same or subsequent nights as these coral species, we hypothesize that this opportunistic feeding behavior takes advantage of lipid‐rich coral gamete bundles to recover energy reserves expended by the brittle star during gametogenesis. The consumption of coral gametes by adult brittle stars suggests an underexplored trophic link between reef invertebrates and also provides evidence that ophiuroid–coral symbioses may oscillate between commensalism and parasitism depending on the ontogeny and reproductive status of both animals. Our observations provide insights into the nuanced, dynamic associations between coral reef invertebrates and may have implications for coral reproductive success and resilience.


| INTRODUC TI ON
Most reef-building scleractinian coral species reproduce through broadcast spawning, whereby gametes are released into the water column for external fertilization (Baird et al., 2009). In many cases, multiple coral species and invertebrate taxa spawn in near synchrony, within minutes or hours of one an other (Babcock et al., , 1986Bouwmeester et al., 2016;Harrison et al., 1984;Van Veghel, 1993).
Mass spawning may have evolved to maximize fertilization success by generating high concentrations of gametes (Levitan et al., 2011;Moláček et al., 2012;, but also as a strategy to minimize predation losses by saturating predator feeding capacity and reducing the impact on any single spawning individual or species (Alino & Col, 1989;Harrison et al., 1984;. On the Great Barrier Reef, planktivorous fish in the families Caesionidae (fusiliers), Chaetodontidae (butterflyfishes), and Pomacentridae (damselfishes) have been found to feed on substantial quantities of coral propagules during mass spawning events (Alino & Col, 1989;Baird et al., 2001;McCormick, 2003;Pratchett et al., 2001;Westneat & Resing, 1988). In the western Atlantic, butterflyfishes have been reported to prey intensely on Diploria labyrinthiformis gamete bundles as they are released (Chamberland et al., 2017;Muller & Vermeij, 2011). Although these trophic links between fish and corals are well established , there are remarkably few publications describing consumption of coral spawn by invertebrates or other marine organisms (Schmahl et al., 2008).
Ophiuroids, commonly known as brittle stars, are among the most biodiverse and prolific invertebrates on Caribbean coral reefs (Kissling & Taylor, 1977;Stöhr et al., 2022). Despite their abundance, these cryptic animals are rarely seen, hidden within the reef structure by day and primarily emerging at night to feed (Birkeland, 1988;Fell, 1966;Hendler et al., 1995;Pomory, 2003). The ruby brittle star, Ophioderma rubicundum, is widely distributed on shallow reefs throughout the western Atlantic (Clark, 1933;Hotchkiss, 1982;Lewis & Bray, 1983;Pomory, 2003). In some locations such as Carrie Bow Cay, Belize, O. rubicundum has been reported among the most numerous ophiuroid species, comprising nearly half of all brittle star specimens collected from fore-reef environments with high living coral cover (Hendler & Pawson, 2000;Hendler & Peck, 1988).
However, this species has been reported at lower abundances (i.e., 0.2 individuals per square meter [Lewis & Bray, 1983]), and is frequently found in reef crest, reef flat, and rubble environments.
They have been described as "opportunistic omnivores" that feed on small organisms, including dinoflagellates, diatoms, foraminiferans, hydroids, polychaetes, crustaceans and mollusks (Binyon, 1972;Reese, 1966). In some cases, O. rubicundum have been reported to exhibit predatory behavior, seizing prey from the benthos or water column by coiling an arm around it before transporting it to the mouth (Birkeland, 1988;Hendler et al., 1995;Reese, 1966;Reimer & Reimer, 1975). Here, we report observations of O. rubicundum capturing and feeding on coral egg-sperm bundles in two locations in the western Atlantic.  (Figure 1b,c). In both coral species, the brittle stars captured multiple gamete bundles at once with one or two arms, using the arm-coil behavior described by Reimer and Reimer (1975).

| Florida Keys, USA, August 2022
On August 17, 2022, six nights AFM, divers from the National Oceanic shows the same brittle star, having emerged completely and perched on the surface of the colony, capturing numerous egg-sperm bundles (Video 1). The brittle star coiled two of its arms around approximately a dozen gamete bundles each, and was observed to move the bundles toward the mouth.

| DISCUSS ION
This report presents rare visual documentation and description of benthic invertebrates consuming gamete bundles during coral spawning events, and represents the first record of this behavior involving multiple coral species and in multiple locations in the western Atlantic.
The specific feeding response we document here-whereby brittle stars coil their arms around gamete bundles-matches how O. rubicundum respond to other high-value food sources. In a laboratory study, O. rubicundum presented with pieces of crab, fish meat, and sea urchin viscerae quickly left their hiding places, moved toward the food source, coiled an arm around it, and transported it to the mouth for ingestion (Reimer & Reimer, 1975). The arm-coiling behavior in our images and footage thus represents a strong feeding response, suggesting that the brittle stars perceive coral gamete bundles as desirable prey items.
Given the nearly concurrent timing of spawning in O. rubicundum and various western Atlantic corals, we hypothesize that Four O. rubicundum feed on Pseudodiploria strigosa gamete bundles as they are released, coiling an arm around the prey before passing it to the mouth.
feeding on coral gamete bundles can supplement the depleted lipid stores of brittle stars and boost metabolic and/or reproductive function (Giese, 1966;Greenfield et al., 1958). On the Great Barrier Reef, planktivorous fishes amass considerable lipid stores as a result of coral gamete consumption . Overall, coral spawning seems to present a convenient and valuable food source to enhance metabolic and/or reproductive output in other reef organisms.
Ophioderma rubicundum live inside reef structures, relying on coral colonies as habitat and shelter during daylight hours (Hendler et al., 1995;Pomory, 2003), and perch atop colonies to release their gametes when they spawn (Schmahl et al., 2008). They are typically  (Hendler, 1984), the ophiuroid has also been found to consume the larvae of the sponge, thus exhibiting characteristics of both mutualism and parasitism (Henkel & Pawlik, 2014). In addition, only larger echinoderms take shelter as commensals on or within coral colonies, as larvae and juveniles are vulnerable to tentacle capture or entanglement with coral mucus (Hendler & Littman, 1986;Lewis & Price, 1975;Yamaguchi, 1974). Similar shifts as organisms age may occur in epizoic bryozoans (e.g., Hippoporidra) and scleractinians living on shells of hermit crabs. As these epizoites grow, they enlarge the internal habitable volume of the shell, prolonging the use of the shell by the growing crab, effectively shifting the role of the epizoite from commensal to mutualist (Taylor, 2009).
These observations of predation on coral gametes by adult brittle stars highlight the complexity of trophic dynamics during ontogeny and represent an understudied pathway of energy transfer among reef invertebrates. In light of these findings, we suggest that further observations be made during coral spawning events, by divers and/or submersible camera traps, to identify whether additional instances of coral gamete consumption have gone undocumented, especially by other invertebrate species that reproduce around the same time as corals.
Most broadcast spawning corals, including O. faveolata and P. strigosa, release gametes on just a few nights per year (Szmant, 1986), limiting their prospects for reproduction. Although reef fish can consume large quantities of coral gametes during mass spawning events (Westneat & Resing, 1988), predation occurs in the water column and is likely to be distributed among the gametes of many colonies.
In contrast, since brittle stars are confined to the surfaces of coral colonies, their feeding is presumably confined to the gamete bundles of the very coral that it is using for shelter, potentially impacting that individual more directly. Although any loss of gametes, by definition, decreases reproductive fitness, the overall impact of ophiuroid predation remains unknown and likely depends on (1) coral colony size, (2) the number of bundles released during a spawning event, (3) how many brittle stars feed on the surface of the coral, and (4) how many bundles each brittle star consumes. Coral fecundity increases disproportionately with colony size (Hall & Hughes, 1996; Álvarez-Noriega F I G U R E 2 Screenshot from video footage depicting Ophioderma rubicundum (circled in white) emerging from its crevice within an Orbicella faveolata colony as the coral begins to spawn off Key Largo, FL in August 2022. Arm-waving behavior from O. rubicundum can be seen as parts of the coral has released gamete bundles, while polyps in the area near the brittle star are still "staging" gamete bundles for release.

V I D E O 1 An adult
Ophioderma rubicundum captures egg-sperm gamete bundles from a spawning Orbicella faveolata colony off Key Largo, FL on 17th August 2022. The brittle star has two arms each coiled around approximately one dozen gamete bundles that were just released from the colony. et al., 2016), likely because smaller colonies invest more energy in somatic growth than reproduction. In large colonies that release thousands of gametes at once, the capture of a few dozen bundles by ophiuroids may be minimally impactful. However, the reproductive success of a smaller colony that releases fewer bundles may diminish considerably if several dozen are eaten upon release, or if multiple brittle stars feed on its surface (as we observed on a P. strigosa colony).
Consequently, future studies should quantify the number of coral gamete bundles that mature brittle stars consume, particularly as a proportion of total colony output.
The two coral species whose gametes were consumed are particularly vulnerable; O. faveolata was listed as "threatened" under the US Endangered Species Act in 2014, and P. strigosa was recently reclassified as "critically endangered" by IUCN (Rodríguez-Martínez et al., 2022), having experienced considerable declines in recent years due to stony coral tissue loss disease (Camacho-Vite et al., 2022). Coral reproduction is already compromised; as the number of potential parent corals declines and spawning becomes less synchronized (Gardner et al., 2003;Levitan & McGovern, 2005;Shlesinger & Loya, 2019), external pressures such as gamete predation may further decrease fertilization success, reduce recruitment, and inhibit community recovery following disturbance . Consequently, trophic interactions be-

DATA AVA I L A B I L I T Y S TAT E M E N T
Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.